Skip to main content

Comparative toxicity of antifouling compounds on the development of sea urchin

Abstract

In the present study, embryotoxicity experiments using the sea urchin Lytechinus variegatus were carried out to better clarify the ecotoxicological effects of tributyltin (TBT) and triphenyltin (TPT) (the recently banned antifouling agents), and Irgarol and Diuron (two of the new commonly used booster biocides). Organisms were individually examined to evaluate the intensity and type of effects on embryo-larval development, this procedure has not been commonly used, however it showed to be a potentially suitable approach for toxicity assessment. NOEC and LOEC were similar for compounds of same chemical class, and IC10 values were very close and showed overlapping of confidence intervals between TBT and TPT, and between Diuron and Irgarol. In addition, IC10 were similar to NOEC values. Regardless of this, the observed effects were different. Embryo development was interrupted at the gastrula and blastula stages at 1.25 and 2.5 μg l−1 of TBT, respectively, whereas pluteus stage was reached with the corresponding concentrations of TPT. Furthermore, embryos reached the prism and morula stages at 5 μg l−1 of TPT and TBT, respectively. The effects induced by Irgarol were also more pronounced than those caused by Diuron. Pluteus stage was always reached at any tested Diuron concentration, while embryogenesis was interrupted at blastula/gastrula stages at the highest concentrations of Irgarol. Therefore, this study proposes a complementary approach for interpreting embryo-larval responses that may be employed together with the traditional way of analysis. Consequently, this application leads to a more powerful ecotoxicological assessment tool focused on embryotoxicity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • ABNT (2006) Ecotoxicologia aquática-Toxicidade crônica de curta duração—“Método de ensaio com ouriço-do-mar (Echinodermata: Echinoidea)”. Norma ABNT-NBR:15350:2006, Associação Brasileira de Normas Técnicas, Rio de Janeiro, 14 p

  • Alzieu C (1998) Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast Manag 40(1):23–36

    Article  Google Scholar 

  • Alzieu C (2000) Impact of tributyltin on marine invertebrates. Ecotoxicology 9(1–2):71–76

    Article  CAS  Google Scholar 

  • ASTM (2004) Standard guide for “Conducting static acute toxicity tests with echinoid embryos”. Standard E1563:1995 (2004), ASTM International, West Conshohocken, PA, 20 p

  • Becker Van-Slooten K, Tarradellas J (1994) Accumulation, depuration and growth effects of tributyltin in the freshwater bivalve Dreissena polymorpha under field conditions. Environ Toxicol Chem 13:755–762

    CAS  Google Scholar 

  • Bellas J (2008) Prediction and assessment of mixture toxicity of compounds in antifouling paints using the sea-urchin embryo-larval bioassay. Aquat Toxicol 88(4):308–315

    Article  CAS  Google Scholar 

  • Bellas J, Beiras R, Marino-Balsa J, Fernandez N (2005) Toxicity of organic compounds to marine invertebrate embryos and larvae: a comparison between the sea urchin embryogenesis bioassay and alternative test species. Ecotoxicology 14(3):337–353

    Article  CAS  Google Scholar 

  • Bresch H, Arendt U (1977) Influence of different organochlorine pesticides on the development of the sea urchin embryo. Environ Res 13(1):121–128

    Article  CAS  Google Scholar 

  • CETESB (1999) Água do mar—“Teste de toxicidade crônica de curta duração com Lytechinus variegatus, Lamarck, 1816”. Norma Técnica L5.250:1999, Companhia de Tecnologia e Saneamento Ambiental, São Paulo, 20 p

  • Chambers LD, Stokes KR, Walsh FC, Wood RJK (2006) Modern approaches to marine antifouling coatings. Surf Coat Technol 201(6):3642–3652

    Article  CAS  Google Scholar 

  • Cima F, Ballarin L, Bressa G, Martinucci G, Burighel P (1996) Toxicity of organotin compounds on embryos of a marine invertebrate (Styela plicata; Tunicata). Ecotoxicol Environ Saf 35(2):174–182

    Article  CAS  Google Scholar 

  • Cornelis C, Bierkens J, Joris I, Nielsen P, Pensaert S (2006) Quality criteria for re-use of organotin-containing sediments on land. J Soils Sediments 6(3):156–162

    Article  Google Scholar 

  • Crane M, Newman MC (2000) What level of effect is a no observed effect? Environ Toxicol Chem 19(2):516–519

    Article  CAS  Google Scholar 

  • dema-Hannes R, Shenker J (2008) Acute lethal and teratogenic effects of tributyltin chloride and copper chloride on mahi mahi (Coryphaena hippurus) eggs and larvae. Environ Toxicol Chem 27(10):2131–2135

    Article  Google Scholar 

  • Dimitriou P, Castritsi-Catharios J, Miliou H (2003) Acute toxicity effects of tributyltin chloride and triphenyltin chloride on gilthead seabream, Sparus aurata L., embryos. Ecotoxicol Environ Saf 54(1):30–35

    Article  CAS  Google Scholar 

  • Downs C, Downs A (2007) Preliminary examination of short-term cellular toxicological responses of the coral Madracis mirabilis to acute irgarol 1051 exposure. Arch Environ Contam Toxicol 52(1):47–57

    Article  CAS  Google Scholar 

  • Drifmeyer J (1981) Urchin Lytechinus variegatus grazing on Eelgrass, Zostera marina. Estuar Coasts 4(4):374–375

    Article  Google Scholar 

  • Duft M, Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J (2003) Toxicity of triphenyltin and tributyltin to the freshwater mudsnail Potamopyrgus antipodarum in a new sediment biotest. Environ Toxicol Chem 22(1):145–152

    CAS  Google Scholar 

  • Environment Canada (1997) Biological Test Method: “Fertilization assay using echinoids (sea urchin and sand dollars)”. Report EPS1/RM/27:(1992)1997, Ottawa, Ontario, Canada, 97 p

  • Evans SM, Birchenough AC, Brancato MS (2000) The TBT ban: out of the frying pan into the fire? Mar Pollut Bull 40(3):204–211

    Article  CAS  Google Scholar 

  • Fent K (1996) Ecotoxicology of organotin compounds. Crit Rev Toxicol 26(1):3–117

    Article  Google Scholar 

  • Fernandez-Alba AR, Hernando MD, Piedra L, Chisti Y (2002) Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal Chim Acta 456(2):303–312

    Article  CAS  Google Scholar 

  • Girard JP, Ferrua C, Pesando D (1997) Effects of tributyltin on Ca2+ homeostasis and mechanisms controlling cell cycling in sea urchin eggs. Aquat Toxicol 38(4):225–239

    Article  CAS  Google Scholar 

  • Hall LW, Giddings JM, Solomon KR, Balcomb R (1999) An ecological risk assessment for the use of Irgarol 1051 as an algaecide for antifoulant paints. Crit Rev Toxicol 29(4):367–437

    CAS  Google Scholar 

  • Harino H, Langston, WJ (2009) Degradation of alternative biocides in the aquatic environment. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Tokyo,Japan, pp 397–412

  • Harino H, Fukushima M, Kawai S (1999) Temporal trends of organotin compounds in the aquatic environment of the Port of Osaka, Japan. Environ Pollut 105:1–7

    Article  CAS  Google Scholar 

  • His E, Heyvang I, Geffard O, De Montaudouin X (1999) A comparison between oyster (Crassostrea gigas) and sea urchin (Paracentrotus lividus) larval bioassays for toxicological studies. Water Res 33(7):1706–1718

    Article  CAS  Google Scholar 

  • Hoch M (2001) Organotin compounds in the environment—an overview. Appl Geochem 16(7–8):719–743

    Article  CAS  Google Scholar 

  • IMO (2008) International convention on the control of harmful anti-fouling systems on ships. http://www.imo.org/conventions/mainframe. Accessed 17 September 2008

  • Isnard P, Flammarion P, Roman G, Babut M, Bastien P, Bintein S, Essermeant L, Ferard JF, Gallotti-Schmitt S, Saouter E, Saroli M, Thiebaud H, Tomassone R, Vindimian E (2001) Statistical analysis of regulatory ecotoxicity tests. Chemosphere 45(4–5):659–669

    Article  CAS  Google Scholar 

  • Koike I, Mukai H, Nojima S (1987) The role of the sea urchin, Tripneustes gratilla (Linnaeus), in decomposition and nutrient cycling in a tropical seagrass bed. Ecol Res 2(1):19–29

    Article  Google Scholar 

  • Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30(2):235–248

    Article  CAS  Google Scholar 

  • Kotrikla A (2009) Environmental management aspects for TBT antifouling wastes from the shipyards. J Environ Manage 90:S77–S85

    Article  CAS  Google Scholar 

  • Langston WJ, Harino H, Pope ND (2009) Behaviour of organotins in the coastal environment. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, New York, pp 75–94

    Chapter  Google Scholar 

  • Manzo S, Buono S, Cremisini C (2006) Toxic effects of irgarol and diuron on sea urchin Paracentrotus lividus early development, fertilization, and offspring quality. Arch Environ Con Tox 51(1):61–68

    Article  CAS  Google Scholar 

  • Marin MG, Moschino V, Cima F, Celli C (2000) Embryotoxicity of butyltin compounds to the sea urchin Paracentrotus lividus. Mar Environ Res 50(1–5):231–235

    Article  CAS  Google Scholar 

  • Mastroti RR, Sousa ECPM, Abessa DMS (2001) Toxicidade de tensoativos aniônicos sobre embriões de ouriço do mar Lytechinus variegatus. In: Moraes R, Crapez M, Pfeiffer W, Farina M, Bainy A, Teixeira V (eds) Efeitos de poluentes sobre organismos marinhos. Arte & Ciência Villipres, São Paulo, SP, pp 207–216

    Google Scholar 

  • Michel P, Averety B, Andral B, Chiffoleau J, Galgani F (2001) Tributiltin along the coasts of Corsica (Western Mediterranean): a persistent problem. Mar Pollut Bull 42(11):1128–1132

    Article  CAS  Google Scholar 

  • Mochida K, Fujii K (2009) Further effects of alternative biocides on aquatic organisms. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo,Japan, pp 383–395

    Chapter  Google Scholar 

  • Moschino V, Marin MG (2002) Spermiotoxicity and embryotoxicity of triphenyltin in the sea urchin Paracentrotus lividus Lmk. Appl Organometal Chem 16(4):175–181

    Article  CAS  Google Scholar 

  • Nipper MG, Prósperi VA, Zamboni AJ (1993) Toxicity testing with coastal species of southeastern Brazil—echinoderm sperm and embryos. Bull Environ Contam Toxicol 50(5):646–652

    Article  CAS  Google Scholar 

  • Norberg-King TJ (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (Icp) Approach version 2.0. National Effluent Toxicity Assessment Center, Environmental Research Laboratory, Duluth, MN, Technical Report 63–93

  • Pinsino A, Matranga V, Trinchella F, Roccheri MC (2010) Sea urchin embryos as an in vivo model for the assessment of manganese toxicity: developmental and stress response effects. Ecotoxicology 19(3):555–562

    Article  CAS  Google Scholar 

  • Piver WT (1973) Organotin compounds: industrial applications and biological investigation. Environ Health Persp 4:61–79

    Article  CAS  Google Scholar 

  • Raffray M, Mccarthy D, Snowden RT, Cohen GM (1993) Apoptosis as a mechanism of tributyltin cytotoxicity to thymocytes: relationship of apoptotic markers to biochemical and cellular effects. Toxicol Appl Pharm 119(1):122–130

    Article  CAS  Google Scholar 

  • Ranke J, Jastorff B (2000) Multidimensional risk analysis of antifouling biocides. Environ Sci Pollut Res 7(2):105–114

    Article  CAS  Google Scholar 

  • Ranke J, Jastorff B (2002) Risk comparison of antifouling biocides. Fresen Environ Bull 11(10A):769–772

    CAS  Google Scholar 

  • Reader S, Moutardier V, Denizeau F (1999) Tributyltin triggers apoptosis in trout hepatocytes: the role of Ca2+, protein kinase C and proteases. Biochim Biophys Acta (BBA)—Mol Cell Res 1448(3):473–485

    Article  CAS  Google Scholar 

  • Ringwood AH (1992) Comparative sensitivity of gametes and early developmental stages of a sea-urchin species (Echinometra mathaei) and a bivalve species (Isognomon californicum) during metal exposures. Arch Environ Con Toxcol 22(3):288–295

    CAS  Google Scholar 

  • Rüdel H (2003) Case study: bioavailability of tin and tin compounds. Ecotoxicol Environ Saf 56(1):180–189

    Article  Google Scholar 

  • Serafy DK (1973) Variation in the polytypic sea urchin Lytechinus Variegatus (Lamarck, 1816) in the Western Atlantic (Echinodermata; Echinoidea). Bull Mar Sci 23:525–534

    Google Scholar 

  • Takeuchi I, Takahashi S, Tanabe S, Miyazaki N (2004) Butyltin concentrations along the Japanese coast from 1997 to 1999 monitored by Caprella spp. (Crustacea: Amphipoda). Mar Environ Res 57(5):397–414

    Article  CAS  Google Scholar 

  • Thomas KV, Fileman TW, Readman JW, Waldock MJ (2001) Antifouling paint booster biocides in the UK coastal environment and potential risks of biological effects. Mar Pollut Bull 42(8):677–688

    Article  CAS  Google Scholar 

  • USEPA (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to marine and estuarine organisms. EPA-821-R-02-014, 3rd edition, U.S. Environmental Protection Agency, Office of Water, Washington, DC, p 464

  • Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD, Orth RJ, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 463–501

    Chapter  Google Scholar 

  • Valentine JF, Heck KL (1991) The role of sea urchin grazing in regulating subtropical seagrass meadows: evidence from field manipulations in the northern Gulf of Mexico. J Exp Mar Biol Ecol 154(2):215–230

    Article  Google Scholar 

  • Van der Hoeven N (2004) Current issues in statistics and models for ecotoxicological risk assessment. Acta Biotheor 52(3):201–217

    Article  Google Scholar 

  • Voulvoulis N, Scrimshaw MD, Lester JN (1999) Alternative antifouling biocides. Appl Organomet Chem 13(3):135–143

    Article  CAS  Google Scholar 

  • Watts SA, McClintock JB, Lawrence JM (2001) The ecology of Lytechinus variegatus. In: John ML (ed) Developments in aquaculture and fisheries science edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 375–393

    Chapter  Google Scholar 

  • Zhang ZB, Hu JY, Zhen HJ, Wu XQ, Huang C (2008) Reproductive inhibition and transgenerational toxicity of triphenyltin on medaka (Oryzias latipes) at environmentally relevant tip levels. Environ Sci & Technol 42(21):8133–8139

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Petrobras S.A. for the infrastructure built (Research grant No. 4600224067) at CONECO Laboratory (FURG-RS), and to colleagues Ítalo Braga de Castro and Luís Alberto Echenique Dominguez for help in the chemical analyses. F. C. Perina (MSc grant No. 134170/2007-5), D. M. S. Abessa (PQ 303620/2008-0) and G. Fillmann (PQ 311459/2006-4 and 314335/2009-9) were sponsored by CNPq (Brazilian National Research Council).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Fernando Cesar Perina.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Perina, F.C., de Souza Abessa, D.M., Pinho, G.L.L. et al. Comparative toxicity of antifouling compounds on the development of sea urchin. Ecotoxicology 20, 1870–1880 (2011). https://doi.org/10.1007/s10646-011-0725-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0725-y

Keywords

  • Antifouling
  • Aquatic pollutant
  • Assessment tool
  • Ecotoxicology
  • Embryo-larval response
  • Embryogenesis